Nematode Parasites of Brazilian Piciformes Birds: a General Survey with Description of Procyrnea Anterovulvata N

Home , Aracari, Bucco, Diplotriaenidae, Habronematoidea, Little woodpecker, Monasa

Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(4): 479-487, Jul./Aug. 1996 479 Nematode Parasites of Brazilian Piciformes Birds: a General Survey with Description of Procyrnea anterovulvata n. sp. (Habronematoidea, Habronematidae) Roberto Magalhães Pinto+, J Júlio Vicente, Dely Noronha Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil Thirty species of nematodes recovered from Piciformes hosts are reported. Procyrnea anterovulvata n. sp. from Chelidoptera tenebrosa brasiliensis is described and compared to P. colaptes and P. pileata. The considered morphometric parameters are mainly related to the ratio between length of the body/ distance of the vulva to the anterior end. It is approximately 1:0.5 in P. colaptes and P. pileata compared to 1:0.1 in the new species. The male of Synhimantus (Dispharynx) crassissima is described for the first time. Thelazia ( Thelaziella) spizaeti is revalidated and new records are reported for some species.

Key words: nematodes - Procyrnea anterovulvata n. sp. - new records - Piciformes - birds - Brazil

The nematodes identified during the present in- tracheolopyrus (Malherbe); 1 Picumnus cirratus vestigation parasitize a great number of hosts, dis- maconelli Sharpe. RAMPHASTIDAE: 3 tributed in four families of Piciformes birds. Pteroglossus aracari aracari L.; 3 Ramphastos This survey was scheduled to provide further tucanus tucanus L. data on morphometrics, host records and geo- Nematodes were preserved in Railliet & graphical distribution for the nematode parasites Henry’s solution (0.85% NaCl solution: 93 ml; of jacamars, puffbirds, toucans and woodpeckers formaldehyde: 5 ml; glacial acetic acid: 2 ml) and in Brazil. were processed for study as described elsewhere MATERIALS AND METHODS (Pinto et al. 1993). Preparation of “en face” mounts was done ac- Seventy-four samples of nematodes, recovered cording to Anderson (1958). Illustrations were pre- between 1913 and 1963 in Brazilian North, Cen- pared with a drawing tube connected to an Olympus tral and Southeastern regions during institutional light microcope. Measurements are in microme- scientific expeditions and deposited in the ters, unless otherwise indicated. NHR and NGD Helminthological Collection of the Oswaldo Cruz indicate New Host Record and New Geographical Institute (CHIOC), were studied. The number of Distribution, respectively. Classification of the examined specimens, according to host family is: nematodes follow Anderson and Bain (1976), BUCCONIDAE: 6 Chelidoptera tenebrosa Chabaud (1975 a, b, 1978) and confirmation of the brasiliensis Sclater; 3 Monasa nigrifrons taxonomic status of the hosts was based on Pinto nigrifrons (Spix); 5 Notharchus macrorhynchos (1978) and Sick (1984). swainsoni (G. R. Gray); 1 Nystalus chacuru chacuru (Vieillot); 11 Nystalus maculatus RESULTS maculatus (Gmelin). GALBULIDAE: 2 Galbula (Habronematoidea, Habronematidae, ruficauda rufoviridis Cabanis. PICIDAE: 15 Celeus Habronematinae) flavescens flavescens (Gmelin); 11 Celeus Procyrnea anterovulvata n. sp. flavescens lugubris (Malherbe); 2 Celeus jumana ( Fig. 1 a-f ) jumana (Spix); 6 Phloeoceastes melanoleucos Description: morphometrics based on five melanoleucos (Gmelin); 3 Phloeoceastes robustus specimens, two males and three females. (Lichtenstein); 1 Phloeoceastes rubricollis Males (Fig. 1 d, e): body 4.99-5.18 mm long, 150-160 wide. Mouth with two lips with three pedunculate papillae each, two small, lateral in the outer circle and one large, central in the inner; two interlabia present. Oral aperture nearly round. Buc- +CNPq research fellow Proc. no. 300374/80-1. Fax: 55- 21-260.4866 cal capsule with thick sclerotized lining, 32-39 Received 7 November 1995 long. Muscular and glandular esophagus 300-320 Accepted 6 May 1996 and 1.58-1.63 mm long, respectively. Nerve ring 480 Nematode Parasites of Brazilian Piciformes Birds RM Pinto et al.

Fig. 1: Procyrnea anterovulvata n. sp. – a: anterior portion of female, ventral view. b: anterior extremity of female, lateral view. c: head of female, en face view. d: posterior extremity of male, ventral view. e: posterior portion of male, ventro-lateral view. f: posterior extremity of female, lateral view. Bars: 0.02 mm in Fig. c; 0.1 mm in Figs b, d, f; 0.2 mm in Fig. e; 0.5 mm in Fig. a.

180 from anterior extremity. Excretory pore not absent. Eleven pairs of pedunculate caudal papil- observed. Left spicule slender, 1.56-1.62 mm long. lae, of which four pairs are pre- and seven post- Right spicule stouter, 240-270 long. Gubernaculum cloacal, supported by large and prominent caudal Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(4), Jul./Aug. 1996 481 alae. Cloacal aperture 110-130 from posterior ex- (Acuarioidea, Acuariidae, Acuariinae) tremity. Synhimantus (Dispharynx) crassissima (Molin, Females (Fig. 1 a, b, c, f ): body 12.24-12.75 1860) Chabaud, 1975 mm long, 220-260 wide. Mouth and buccal cap- ( Fig. 2 a-c ) sule as in males; buccal capsule 39-46 long. Mus- Morphometrics: based on seven specimens, cular and glandular esophagus 320-340 and 2.03- four males and three females, recovered from 2.17 mm long, respectively. Nerve ring 180 from Ramphastos t. tucanus. anterior extremity. Excretory pore not observed. Description: males (Fig. 2 b ): body 6.51-8.62 Vulva 1.68-1.96 mm from anterior extremity. Va- mm long, 220-300 wide. Mouth with two large gina 1.54-1.68 mm long. Eggs 50-54 long, 28-32 papilliform lips. Oral aperture oval-elongate, near wide. Anus 120-130 from posterior extremity. of which derives two pairs of cephalic cordons. Taxonomic summary Buccal capsule 120-170 long. Cephalic cordons thick, markedly flexed, strongly recurrent, not anas- Type host: Chelidoptera tenebrosa brasiliensis; tomosing, 730-770 long. Muscular and glandular common name: swallow-wing (“andorinha, miolinho, urubuzinho”) esophagus 680-720 and 2.03-2.45 mm long, respectively. Nerve ring 280-300 from anterior ex- Site of infection: gizzard tremity. Excretory pore not observed. Left spicule Type locality: Conceição da Barra, State of Espírito Santo, Brazil slender, 460-500 long. Right spicule stouter, 190- 210 long. Gubernaculum absent. Ten pairs of Specimens studied: CHIOC no. 32,783 d (alotype), pedunculate caudal papillae, of which four are pre- 32,783 a (holotype), 32,783 b, c, e, f (paratypes) (whole mounts); 14,811 (wet material). and six post-cloacal, supported by narrow caudal alae. Cloacal aperture 210-270 from posterior ex- Etymology: the specific name derives from the tremity. Latin anterior + vulva, meaning “which posseses the vulva in the anterior portion of the body”. Redescription: females (Fig. 2 a, c): body 7.65- 9.53 mm long, 570-580 wide. Mouth and oral ap- Remarks erture as referred for the males. Buccal capsule 140- The species of Procyrnea Chabaud, 1975 180 long. Cephalic cordons as referred for the present the vulvar aperture in the middle portion males, 680 long. Muscular and glandular esopha- of the body (Chabaud 1958), slightly pre- or post- gus 510-680 and 1.96-2.38 mm long, respectively. equatorial. Nevertheless, the ratio between length Nerve ring 280-300 from anterior extremity. Ex- of the body/distance of vulva to the anterior end is cretory pore not observed. Vulva in posterior part approximately 1:0.5 in all previously described spe- of the body, 570-930 from posterior extremity. cies of the genus. Ovijector 210 long. Eggs 39-43 long, 25-28 wide. According to Chabaud and Brygoo (1958), two Anus 120-160 from posterior extremity. species of Procyrnea parasitize Piciformes hosts: P. colaptes (Walton, 1923) Chabaud, 1975, in Taxonomic summary which the above mentioned ratio is of 1:0.49-0.58 Hosts: Chelidoptera tenebrosa brasiliensis NHR; (present data) and P. pileata (Walton, 1928) Notharchus macrorhynchus swainsoni (= Bucco Chabaud, 1975 with ratio of 1:0.47-0.59 (Walton swainsoni); common name: spotted puffbird 1928). Both species are reported from USA, para- (“macuru”) - NHR; Ramphastos t. tucanus (= sitizing Colaptes auratus luteus Bangs and Ramphastos monilis); common name: red-billed Hylotomus pileatus, respectively (Walton 1923, toucan (“tucano de peito branco, quirina, pia- 1928, Cram 1927). pouco”) - NHR Procyrnea anterovulvata n. sp. is compared to Other Piciformes host: Ramphastos vitellinus these two species based on the high specificity of Lichtenstein, according to Cram (1927) this group of nematodes to this order of birds. In Site of infection: gizzard the new species the ratio between lenght of body/ Localities: Angra dos Reis, State of Rio de Janeiro; distance of the vulva to the anterior end is of Belém, State of Pará; and Engano, State of Espírito 1:0.13-0.15, clearly distinguishing P. anterovulvata Santo, Brazil n. sp. from P. colaptes and P. pileata, as well as Specimens studied: CHIOC no. 32,778, 32,779 a- from the other species actually included in the ge- b, 32,780 a-h (whole mounts). nus. Moreover, the right spicule in males of P. Remarks anterovulvata n. sp. is remarkably shorter (240- This species was originally described as 270) in comparison with the observed in P. Dispharagus crassissimus in 1860 from a Brazil- colaptes and P. pileata (390-410 and 440, re- ian toucan based on female specimens and was spectively). redescribed by Cram (1927) as Dispharynx 482 Nematode Parasites of Brazilian Piciformes Birds RM Pinto et al. crassissima also considering female specimens (Thelazioidea, Thelaziidae, Thelaziinae) only. Males were referred as “unknown” by both Thelazia (Thelaziella) spizaeti Strachan, 1957 authors. The present data refer to the first descrip- (Fig. 2 d-f) tion of male of this species. Taxonomic summary (Seuratoidea, Seuratidae, Seuratinae) Host: Pteroglossus a. aracari; common name: Skrjabinura spiralis Gnédina, 1933 black-necked aracari (“araçari”) - NHR Taxonomic summary Site of infection: orbital cavity Host: Galbula ruficauda rufoviridis; common Locality: Raul Soares, State of Minas Gerais, Bra- zil name: rufous-tailed jacamar (“beija-flor grande, Specimens studied: CHIOC no. 32,782 a-c (whole cuitelão”) - NHR Site of infection: intestine mounts). Locality: Salobra, State of Mato Grosso do Sul, Remarks Brazil Thelazia spizaeti, proposed from Spizaetus Specimen studied: CHIOC no. 32,777 (whole ornatus (Daudin), a Brazilian accipitrid hawk mount). (Strachan 1957), is revalidated herein. It was con- Remarks sidered a synonym of T. (Thelaziella) aquilina Baylis, 1934 by Anderson and Diaz-Ungria (1959) This species was referred in other hosts than that may have misunderstood reliable morphomet- Piciformes and its taxonomic status had also been discussed by Pinto et al. (1994), when Skrjabinura ric data on T. (T.) spizaeti, mainly those related to the spicules. In T. (T.) aquilina they are 0.17-0.18 magnum (Johnston & Mawson, 1941) Mawson, and 1.7-2.0 mm long, compared to 0.14 and 0.24 1960 was proposed as a junior synonym of S. spiralis, reported parasitizing Falconidae birds in mm in T. (T.) spizaeti. This extreme variation in the spicular ratio (1: Brazil. 1.7-10.0) should not be considered an interspecific (Subuluroidea, Subuluridae, Subulurinae) variation even though the specimens have been Subulura travassosi Barreto, 1918 recovered from different hosts. Taxonomic summary Procyrnea colaptes (Walton, 1923) Chabaud, Hosts: Chelidoptera tenebrosa brasiliensis, 1975 Monasa n. nigrifrons; common name: black- Taxonomic summary fronted nunbird (“bico de brasa”) - NHR; Hosts: Celeus flavescens lugubris; common name: Notharchus macrorhynchos swainsoni - NHR; pale-crested woodpecker (“pica-pau amarelo”) - Nystalus c. chacuru (= Bucco chacuru); common NHR; C. j. jumana; common name: chestnut wood- name: white-eared puffbird (“joão-bobo, dormião, pecker (“pica-pau castanho”) - NHR jacuru, paulo-pires”); Nystalus m. maculatus; com- Site of infection: gizzard mon name: spot-backed puffbird (“bico de latão”) Locality: Salobra, State of Mato Grosso do Sul, - NHR Brazil-NGD Other Piciformes hosts: Bucco collaris Lath., B. Specimens studied: CHIOC no. 32,785 a-i (whole rufiventris Natt., B. t. tamatia Gm, Malacoptila mounts), 11,605, 12,778, 20,705 (wet material). torquata (Hahn & Kust), Monasa atra (Bodd.), M. Remarks m. morphoeus (Hahn & Kust), M. nigra (Müller), Nonnula r. rubecula (Spix), Notharchus m. Comments on this species are under the “Re- marks” for Procyrnea anterovulvata n. sp. macrorhynchos (Gmelin), N. t. tectus (Bodd.), Nystalus s. striolatus (Pelz.), according to Barreto Procyrnea pileata (Walton, 1928) Chabaud, (1919). 1975 Site of infection: intestine Taxonomic summary Localities: Angra dos Reis, State of Rio de Janeiro; Hosts: Celeus f. flavescens; common name: blond- Cachimbo, State of Pará; Conceição da Barra, State crested woodpecker (“pica-pau amarelo”) - NHR; of Espírito Santo; Salobra and Bodoquena, State C. flavescens lugubris - NHR; C. j. jumana - NHR; of Mato Grosso do Sul; Ilha Seca and Rincão, State Phloeoceastes m. melanoleucos; common name: of São Paulo, Brazil crimson-crested woodpecker (“pica-pau real”) - Specimens studied: CHIOC no. 3,299, 4,981, NHR; P. robustus; common name: robust wood- 6,166, 11,742, 11,775, 11,776, 12,589, 12, 595, pecker (“pica-pau, pinica pau”) - NHR; P. 12, 596, 12,628, 13, 051, 13,282, 14,782, 14,793, rubricollis trachelopyrus; common name: red- 14,837, 15,596, 20,937, 21,420, 21,441 (wet necked woodpecker (“pica-pau do peito material). Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(4), Jul./Aug. 1996 483

Fig. 2: Synhimanthus (Dispharynx) crassissima – a: anterior extremity of female, ventral view. b: posterior portion of male lateral view. c: posterior portion of female, lateral view. Thelazia (Thelaziella) spizaeti – d: posterior extremity of female, lateral view. e: anterior portion of female, lateral view. f: posterior portion of male, lateral view. Bars: 0.1 mm in all Figs. 484 Nematode Parasites of Brazilian Piciformes Birds RM Pinto et al. vermelho”) - NHR; Picumnus cirratus maconelli; Other Piciformes hosts: Campephilus common name: white-barred piculet (“picapau- melanoleucos (Gmelin), Campylorhamphus zinho barrado”) - NHR; Ramphastos t. tucanus - procurvoides (Lafrenaye), Ramphastos tucanus L. NHR and Veniliornis passerinus olivinus (Natterer & Site of infection: gizzard Malherbe), according to Bartlett and Greiner Localities: Angra dos Reis, State of Rio de Janeiro; (1986) Belém and Cachimbo, State of Pará; Salobra, State Site of infection: among tendons of feet of Mato Grosso do Sul; Soóretama, State of Locality: Raul Soares, State of Minas Gerais, Bra- Espírito Santo, Brazil - NGD zil Specimens studied: CHIOC no. 32,781 a-c, 32,786 Specimens studied: CHIOC no. 20,064 (wet mate- a-b (whole mounts), 5,386, 5,424, 13,020, rial) 13,064, 13,310, 13,486, 20,535, 20,536, 29,481, Remarks 29,483 (wet material). Pelecitus helicinus is a very common species, Remarks parasitizing a wide range of avian hosts. Morpho- Comments on this species are under the “Re- metric data on this nematode have been recently marks” for Procyrnea anterovulvata n. sp. reported (Pinto et al. 1993). (Diplotriaenoidea, Diplotriaenidae, Procyrnea sp. Dicheilonematinae) Taxonomic summary Hamatospiculum insigne (Schneider, 1866) Skrjabin, 1916 Hosts: Chelidoptera tenebrosa brasiliensis, Celeus flavescens lugubris, C. j. jumana Taxonomic summary Site of infection: gizzard Hosts: Celeus f. flavescens - NHR; Phloeoceastes Localities: Belém, State of Pará; Salobra and robustus - NHR Bodoquena, State of Mato Grosso do Sul; Ilha Seca, Site of infection: body cavity State of São Paulo, Brazil Localities: Barranco Alto, State of Mato Grosso Specimens studied: CHIOC no. 11,497, 11,587, do Sul; Engano and Soóretama, State of Espírito 11,634, 11,679, 12,444, 12,779, 13,004, 13,178, Santo, Brazil 13,484, 15,021 (wet material). Specimens studied: CHIOC no. 32,784 (whole mount); 14,859, 15,575 (wet material). Remarks The specimens could not be specifically iden- Remarks tified due to their poor state of preservation. This species, the type of the genus, has been reported in Picus sp. from Brazil and Paraguay. It Synhimantus (Dispharynx) sp. was properly figured by Yorke and Maplestone Taxonomic summary (1926) based on Skrjabin (1916). Host: Veniliornis passerinus olivinus; common ( Filarioidea, Onchocercidae, Dirofilariinae ) name: little woodpecker (“pica-pau pequeno”) Pelecitus circularis (Molin, 1860) Railliet & Site of infection: gizzard Henry, 1910 Locality: Angra dos Reis, State of Rio de Janeiro, Brazil Taxonomic summary Specimens studied: CHIOC no. 10,425 (wet mate- Host: Phloeoceastes m. melanoleucos - NHR rial). Site of infection: among tendons of feet Locality: Salobra, State of Mato Grosso do Sul, Remarks Brazil The specimens could not be specifically iden- Specimens studied: CHIOC no. 11,514, 13,019 tified due to their poor state of preservation. (wet material). (Aproctoidea, Aproctidae, Aproctinae) Remarks Aprocta sp. Pelecitus circularis, recently redescribed (Pinto Taxonomic summary et al. 1993), has been referred in a few Brazilian Hosts: Phloeoceastes robustus, Pteroglossus a. birds other than Piciformes (Bartlett & Greiner aracari 1986). Site of infection: body cavity Pelecitus helicinus (Molin, 1860) Railliet & Locality: Barranco Alto, State of Mato Grosso do Henry, 1910 Sul; Soóretama, State of Espírito Santo, Brazil Taxonomic summary Specimens studied: CHIOC no. 15,568, 29,482 Host: Pteroglossus a. aracari - NHR (wet material). Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(4), Jul./Aug. 1996 485 Remarks Locality: Salobra, State of Mato Grosso do Sul, The specimens could not be specifically iden- Brazil tified due to their poor state of preservation. Specimens studied: 32,787 a-b (whole mounts) (Filarioidea,Onchocercidae, Splendidofilariinae) Remarks Splendidofilaria sp. The specimens could not be specifically iden- Taxonomic summary tified due to their poor state of preservation. The nematode species presently reported as Host: Nystalus m. maculatus well as those previously referred in Brazilian Site of infection: body cavity Piciformes hosts are included in Table.

TABLE Nematodes from Piciformes birds in Brazil Parasite species Host species Aprocta sp. Phloeoceastes robustus *Capillaria columbae (Rudolphi, 1819) Ramphastos toco Muller *C. venusta Freitas and Mendonça , 1958 Petroglossus a. aracari L. P. aracari wiedii Sturm Ramphastos toco Muller R. vitellinus ariel Vigors *Cerastospira thriponaxis Wehr, 1930 R. c. culminatus Gould *Dessetfilaria braziliensis (Yeh, 1932) R. dicolorus L. *Dicheilonema fusiformis (Molin, 1858) Monasa tranquila (?) *Diplotriaena sp. Celeus flavescens lugubris Tripsurus flavifrons (Vieill.) *Eulimdana micropenis (Trav., 1926) Selenidera maculirostris (Lich.) *Habronema unilateralis (Molin, 1860) S. maculirostris Ramphastos monilis Muller Hamatospiculum insigne Celeus f. flavescens Phloeoceastes robustus *Oxyspirura anacanthura (Molin, 1860) Ramphastos c. culminatus *O. sygmoidea (Molin, 1860) R. toco cuvieri Wagler *Paronchocerca ibanezi (Freitas, Vicente and Pinto, 1970) Colaptes campestris (Vieill.) Pelecitus circularis Phloeceastes m. melanoleucos P. helicinus Campephilus melanoleucos Campylorhampus procurvoides Pteroglossus a. aracari Ramphastos tucanus Veniliornis passerinus olivinus Procynea anterovulvata n.. sp. Chelidoptera tenebrosa brasiliensis P. colaptes Celeus flavescens lugubris C. j. jumana P. pileata C. f. flavescens C. f. lugubris C. j. jumana Phloeoceastes m. melanoleucos P. robustus P. rubricollis tracheolopyrus Picumnus cirratus maconelli Ramphastos tucanus Procyrnea sp. Chelidoptera tenebrosa brasiliensis Celeus flavescens lugubris C. j. jumama Skrjabinura spiralis Galbula ruficauda rufoviridis * Splendidofiilaria gedoelsti Trav., 1926 Selenidera maculirostris Splendidofilaria sp. Nystalus m. maculatus cont... 486 Nematode Parasites of Brazilian Piciformes Birds RM Pinto et al.

* Subulura strongylina (Rud., 1819) Bucco melanoleuchus (?) Subulura travassosi B. collaris B. rufiventris B. t. tamatia Chelidoptera tenebrosa brasiliensis Malacoptila torquata Monasa atra M. m. morphoeus M. nigra M. n. nigrifrons Nonnula r. rubecula Notharchus m. macrorhynchos N. macrorhynchos swainsoni N. t. tectus Nystalus c. chacuru N. m. maculatus N. s. striolatus Synhimantus (D.) crassissima Chelidoptera tenebrosa brasiliensis Synhimantus (Dispharynx) sp. Veniliornis passerinus olivinus *Tetrameres cruzi Trav., 1914 Notharchus m. macrorhynchos Melanerpes f., flavifrons (Vieill.) *Thelazia anolabiata (Molin,1860) Pteroglossus a. aracari *T. digitata (Molin, 1860) R. toco cuvieri Wagler T. (Thelaziella) spizaeti Pteroglossus a. aracari * Not found during the present study. Data after Yamaguti (1961), Freitas et al. (1970), Anderson and Bain (1976), Vicente et al. (1983), Bartlett et al. (1985), Bartlett and Bain (1987).

ACKNOWLEDGEMENTS Bartlett CM, Wong PL, Anderson RC 1985. Eulimdana lari (Yamaguti, 1935) n. comb. (Nematoda: To Mara Lucia de Souza Lemos, IOC research fel- Filarioidea) from Phalaropus spp. (Charadriiformes) low from the “Setor de Programação Visual (CICT/ in Canada and a review of the genus Eulimdana FIOCRUZ)” for technical support concerning the fig- Founikoff, 1934. J Can Zool 63: 666-672. ures presented. Chabaud AG 1958. Essai de classification des nématodes REFERENCES Habronematinae. Ann Par hum comp 33: 445-508. Anderson RC 1958. Méthode pour l’examen des Chabaud AG 1975a. Keys to the genera of the order nématodes en vue apicale. Ann Par hum comp 33: Spirurida. Camallanoidea, Dracunculoidea, 171-172. Gnathostomatoidea, Physalopteroidea, Anderson RC, Bain O 1976. Keys to the genera of the Rictularioidea and Thelazioidea. p. 1-27. In RC order Spirurida. Diplotriaenoidea, Aproctoidea and Anderson, AG Chabaud, S Willmott (eds). CIH Keys Filarioidea. p. 59-116. In RC Anderson, AG to the nematode parasites of vertebrates 3. Part 1. Chabaud, S Willmott (eds). CIH Keys to the nema- Commomwealth Agricultural Bureaux, England. tode parasites of vertebrates 3. Part 3. Common- Chabaud AG 1975b. Keys to the genera of the order wealth Agricultural Bureaux, England. Spirurida. Spiruroidea, Habronematoidea and Anderson RC, Diaz-Ungria C 1959. Revision preliminar Acuarioidea. p. 29-58. In RC Anderson, AG de las especies de Thelazia Bosc (Spiruroidea: Chabaud, S Willmott (eds). CIH Keys to the nema- Thelaziidae), parasitas de aves. Mem Soc Ci Nat La tode parasites of vertebrates 3. Part 2. Salle 19: 37-75. Commomwealth Agricultural Bureaux, England. Barreto ALBB 1919. Revisão da subfamília Subulurinae Chabaud AG 1978. Keys to the genera of the superfami- Travassos, 1914. Mem Inst Oswaldo Cruz 11: 1-70. lies Cosmocercoidea, Seuratoidea, Heterakoidea and Bartlett CM, Bain O 1987. New avian filarioids Subuluroidea. p. 1-71. In RC Anderson, AG (Nematoda: Splendidofilariinae): Dessetfilaria Chabaud, S Willmott (eds). CIH Keys to the nema- guianensis gen. n. sp. n., Andersonfilaria africanus tode parasites of vertebrates 6. Commomwealth gen. n., sp. n., and Splendidofilaria chandenieri sp. Agricultural Bureaux, England. n. Proc Helminthol Soc Wash 54: 1-14. Chabaud AG, Brygoo ER 1958. Sur un nouveau Bartlett CM, Greiner EC 1986. A revision of Pelecitus nématode habroneme, parasite de rapaces, a Mada- Railliet & Henry, 1910 (Filarioidea, Dirofilariinae) gascar. Mem Inst Sci Madagascar 12: 127-138. and evidence for the “capture” by mammals of Cram EB 1927. Bird parasites of the suborder filarioids from birds. Bull Mus natn Hist nat Paris Strongylata, Ascaridata and Spirurata US Nat Mus 4th ser. 8: 47-99. Bull 140: 1-465. Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(4), Jul./Aug. 1996 487

Freitas JFT, Vicente JJ, Pinto RM 1970. Sobre uma filária Russe Zool 1: 736-757. prodelfa parasita de ave. Atas Soc Biol Rio de Janeiro Strachan AA 1957. Eye worms of the family Thelaziidae 12 (Supl.): 39-42. from Brazilian birds. Can J Zool 35: 179-187. Pinto OMO 1978. Novo catálogo de aves do Brasil 1. Vicente JJ, Pinto RM, Noronha D 1983. Estudo das Empresa Gráfica da Revista dos Tribunais, São espécies brasileiras do gênero Diplotriaena Henry Paulo, 446 pp. & Ozoux, 1909 (Nematoda, Filarioidea). Mem Inst Pinto RM, Vicente JJ, Noronha D 1993. Nematode para- Oswaldo Cruz 78: 165-182. sites of Brazilian psittacid birds, with emphasis on Walton AC 1923. Some new and little known nema- the genus Pelecitus Railliet & Henry, 1910. Mem todes. J Par 10: 60-73. Inst Oswaldo Cruz 88: 279-284. Walton AC 1928. A revision of the Leidy Collection. Pinto RM, Vicente JJ, Noronha D 1994. Nematode para- Proc Acad Nat Sci Philadelphia 79: 49-163. sites of Brazilian accipitrid and falconid birds (Falco- Yamaguti S 1961. Systema Helminthum 3. The nema- niformes). Mem Inst Oswaldo Cruz 89: 359-362. todes of vertebrates. Parts 1 and 2. Interscience Sick H 1984. Ornitologia brasileira, uma introdução. Publishers, New York, 1261 pp. 1. Universidade de Brasília, 474 pp. Yorke W, Maplestone PA 1926. The nematode para- Skrjabin KI 1916. Contributions à l’étude de la faune sites of vertebrates. J A Churchill (eds), London, helminthologique du Paraguay. I. Nématodes. J 536 pp. 488 Nematode Parasites of Brazilian Piciformes Birds RM Pinto et al.